In proposal #155, Alvaro
Jaramillo proposed to split Shy AlbatrossThalassarche
cautainto two or three
species. In that proposal, the most comprehensive recent study of the taxonomy
of albatrosses (and other members of the Procellariiformes), Penhallurick &
Wink 2004 (incorrectly cited as Penhallurick and Wink 2004) was dismissed with
a curt statement that: "there is circularity in the reasoning, as
taxonomic questions that are troubling involve taxa that are allopatric and
have not traditionally been considered good species." This showed scant
respect for, or knowledge of, the use of molecular data to address issues of
taxonomy. The implication of the statement "Using the same dataset"
was that Penhallurick & Wink 2004 was merely a rehash of Nunn and Stanley
(1998). This ignores that fact that Nunn and Stanley (1998) made no use
whatsoever of their data to draw taxonomic conclusions.

Too often in recent
years, ornithologists have shrunk from the precision offered by DNA sequencing
in favour of reasoning involving approximate judgments. In his Recommendation,
Alvaro Jaramillo stated:

"There are two
clear groups (I do think thateremitaandsalviniare sisters), one is theeremita/salvinipair, and the other is thecauta/steadipair, these two groups are
consistently different in morphology, genetics, breeding, and at-sea
distribution, and there is no sign of hybridization although at least one pair
ofsteadihas bred practically in sight of the main
colony oferemita. It is one
data point but a data point nonetheless."

Looking at the grounds
cited by Alvaro, some obvious questions arise. Are "consistent differences
in morphology" grounds for recognising two taxa as two good species?
Hardly, since "consistent differences in morphology" are the minimal
grounds for distinguishing subspecies. We are given no indication of how great
the differences in morphology must be in order to justify separating taxa as
species level rather than subspecies level. The same question attaches to
differences in genetics. How big a difference in genetics justifies recognition
of two taxa as good species rather than subspecies? Alvaro gives no bench-mark.

We are thirdly referred
to differences in "breeding". Earlier, we read that

"breeding times differ somewhat between
taxa
-cautabegins breeding in
early September
-steadibegins breeding in
November
-salvinibreeds Oct-mid
Nov
-eremitabreeds Aug
Sept"

There is an obvious
explanation for the different breeding times: populations breeding further from
the equator breed later.Cautabreeds at Albatross Island 40ˇ23'S, 5,000
breeding pairs; The Mewstone at 43ˇ45'S, 7,000 breeding pairs; and Pedra Branca
at 43ˇ52'S, 200 breeding pairs.Eremitabreeds at the Chatham Islands at 44ˇS,
4,000 breeding pairs.Salvinibreeds at Bounty Islands ca. 47ˇ30' S
76,000 breeding pairs, and at Snares Islands ca. 48ˇ10'S 650 breeding pairs.
Finally,steadibreeds on Auckland Island ca. 50ˇ35'S 3,000
breeding pairs; Disappointment Island 50ˇ35' 72,000 breeding pairs; and Adams
Island 50ˇ35' 100 breeding pairs. It is quite normal with seabirds whose
breeding range extends over many degrees of latitude for those closest to the
equator to breed earlier than those further away. For example, the monotypic
South American TernSterna
hirundinaceabreeds April-Jun
in southeast Brazil; early November in northern Argentina and Uruguay and early
December in southern Argentina. The monotypic Arctic TernSterna paradisaeabreeds May-June in the south of its range,
but July in the north.

Alvaro also appears to
appeal to the fact that different taxa travel to different regions in the
non-breeding period. His account of the non-breeding taxa, which cites no
authority, is much neater than the account in Marchant and Higgins (1990:
304-306). For example, the latter source says oferemita"sedentary or disperse into
central South Pacific". I know of no evidence that indicates thateremita"heads for the Humboldt
Current". His evidence also does not take into account the fact that the
movements of some taxa (for example, "movements of birds from Auckland
Island") are described by Marchant and Higgins as "poorly
known". In any case, I would regard the fact that taxa inhabiting widely
distant breeding islands might utilise different areas as of little taxonomic
significance. Consider the fact that the impact of long-line fishing on
Wandering AlbatrossesDiomedea
exulanshas been much greater on
females than on males because females forage further north. (Carboneras 1992:
211).

Alvaro goes to some
length to establish "Potential Symmetry", citing the fact that one
pair ofsteadihas breed on the Forty-Fours in
the Chatham Island group; that asteadihas visited colonies ofsalvinion the Snares; that a singlesalvinimade a nest in the main colony oferemita; that one pair oferemitahas nested on the Snares, a breeding
site forsalvini; concluding
that "Some of these sympatric breeding events have occurred for various
years in a row." We view such isolated instances, involving one or two
birds, as of no taxonomic significance whatsoever. We are quite happy to
concede that the four taxa are, to all extents and purposes, allopatric. Since
I doubt that Alvaro would wish to claim that allopatry is of itself significant
evidence of species status (we note that nominatecautaand steadi, which Alvaro claims to
be conspecific) are totally allopatric.

We conclude that Alvaro
has not made a convincing case thatcauta(incorporatingsteadi)anderemita/salvinishould be allocated to different species.
We believe that his case for separatingeremitaandsalvini,
in that the two "differ consistently morphologically, genetically and in
their distribution and have not interbred although sympatry has occurred"
is indeed weaker, as he concedes it to be.

Finally, we note that
although Alvaro dismisses Penhallurick and Wink (2004) on the basis of
"circularity", this is inconsistent with his own practice. For
example, he accepts Nunn et al.'s (1996) reorganization of albatross genera,
despite the fact that this was based to a significant extent on a comparison of
differences between within-group and between-group differences. Again, in his
Recommendations, Alvaro several times makes statements referring to, for
example, "the relatively low genetic divergence of this pair,as compared to the others[emphasis added]"; or "The
differences both morphologically and genetically between eremitaandsalviniare much greater than betweensteadiandcauta.
Even so,at least genetically these
two are much more similar to each other than other albatross species pairs.
[emphasis added]" How can Alvaro accuse us of "circularity" when
he makes such statements himself?

Evidence
We unambiguously accept the Multidimensional Biological Species concept in
maintaining the subspecies level to denominate young evolutionary lines, when
they are allopatric and do not differ substantially in morphological or
ecological terms.

We made the following
point in our paper:

"It is our
contention that the calibration of distances between taxa made possible by DNA
sequencing of marker genes makes it possible to obtain more reliable decisions
as to the boundaries between genera, subgenera, species and subspecies. We are
aware that this is not a trivial matter. Issues of technique, and selection of
genes arise. Nonetheless, by examining the distances between well-recognised
subspecies and specieswithina genus, or genera within a family,
especially where there is independent evidence for that status, such as a broad
area of interbreeding between subspecies, we can make soundly based decisions.
"

We also made the
following statement:

"Robertson and
Nunn (1998) did not publish or otherwise provide an input matrix containing the
distance data for the proposed new albatross species, an omission which left
supporters of the Multidimensional BSC uncertain as to whether the proposed
splits were valid within that framework. They did state (1998: 14):
'Idiosyncratically among birds, the level of mitochondrial DNA sequence
divergence between albatross taxa is relatively small compared to their
diagnosable morphological and ecological character differences. Reassuringly,
traditional taxonomic and novel phylogenetic methods are largely supportive of
each other.' This is not enough to resolve the problem of the status of the
proposed splits, given that pairwise distances among traditionally recognised
species within Thalassarcherange
from 3.15% to 1.66%. We also regret the practice in recent years of publishing
only trees, but not the distance matrices on which the trees are based. Tree-generating
packages often generate cladograms with similar terminal branches for taxa
differing by less than 1% and those differing, say, by 5%."

It is our contention
that more attention should be paid to the data in distance matrices rather than
just to the trees generated on the basis of that data. The distance data isprimarydata. The evidence in trees isderiveddata. Furthermore, the evidence of
trees is generally of little help in deciding questions at the level of species
and subspecies. The cytochrome-bmitochondrial
DNA gene is acknowledged as the best gene to sequence for studies at this
level. This is partly because of the faster rate of evolution of mitochondrial
DNA in comparison with nuclear DNA genes. Secondly, cytochrome-bhas been shown to be less susceptible
to multiple substitutions producing homoplasy.

The table below
reproduces the distance data in relation to all members ofThalassarchein our data set. Uncorrected p
distances, derived from complete cytochrome-bsequences, appear below the diagonal.
It should be noted that because the body masses of all members of Thalassarche
are comparable, in terms of the findings of Nunn and Stanley (1998), we should
expect highly similar rates of evolution in all of these taxa.

12

13

14

15

16

17

18

19

20

[12] Thalassarche b. bulleri

[13] T. c. cauta

0.0166

[14] T. c. chlororhynchos

0.0297

0.0271

[15] T. chrysostoma

0.0262

0.0236

0.0262

[16] T. m. melanophris

0.0315

0.0280

0.0280

0.0192

[17] T. chlororhynchos carteri

0.0332

0.0289

0.0035

0.0297

0.0315

[18] T. cauta eremita

0.0201

0.0105

0.0289

0.0236

0.0271

0.0306

[19] T. cauta salvini

0.0192

0.0096

0.0280

0.0227

0.0262

0.0297

0.0026

[20] T. melanophris impavida

0.0289

0.0271

0.0271

0.0201

0.0079

0.0306

0.0280

0.0271

We will list the
uncorrected p distances between each pairing of taxa withinThalassarchein descending order. After each pair,
we will put in brackets an estimate of time of divergence between each pair of
taxa based on the finding that 2% difference in cytochrome-bdistances equates to 1 million years.
These estimates are discussed below.

It will be noticed here
that all the pairs that are 1.66% or more apart represent traditional good
species. All the pairs that are 1.05% or less apart represent what have
traditionally been treated as subspecies. The gap between 1.66% and 1.05% is
the largest in the dataset. It seems sensible to treat this gap as that
cut-off, below which we are dealing with subspecies, and above which, we are
dealing with separate species. We stress that there isno strong evidence that contradicts this
proposal. We concede thatcautaanderemitahave diverged furthest among all the
subspecies within the genusThalassarche.
But classification implies the imposition of boundaries on what in reality is a
continuum. Note that we have here a clear and well justified quantitative
bench-mark, of a type we found to be totally lacking in Alvaro's proposal. Of
course, with our data, it makes no sense to claim thatsalvinianderemitashould be separated at the specific
level. The two taxa withinT.
melanophriswould have a much
stronger claim.

Unfortunately, we did
not have data fromsteadiin our study. But Alvaro himself
concedes that this should be treated as conspecific withcauta. We also note that
Marchant and Higgins (1990:310) stated: "A fourth subspecies,steadifrom Auckland Is., proposed by Falla
(1933) but doubtfully separable fromcautaand validity requires study."

We believe that
comparable data from the other genera with the family Diomedeidae supports our
analysis. Within the genusPhoebastria,
where we have no subspecies, distances between species range from 1.75% betweenPhoebastria nigripesandPhoebastria
immutabilis, to 4.72% betweenPhoebastria
immutabilis andPhoebastria
irrorata. Within the narrowerDiomedea,
we have a distance between the taxa withinD.
exulansand those withinD. epomophoraof 3.3% to 3.6%; within taxa usually
included inD. exulans, we
find distances ranging from 0.00% to 0.89%; the difference betweenD. epomophora epomophoraandD.
epomophora sanfordiis
0.009%, despite the fact that they are distinctly different in appearance and
allopatric. Finally the distance between the two taxa in Phoebetriais 2.10%.

Above, we have used
cytochrome-bdistances to
obtain estimates of time of divergence between taxa. In our paper (2004), we
used amino acid distances. In the original paper, we used the widely accepted
date of 310 mya for the divergence date of diapsid reptiles and synapsid
reptiles to calibrate our amino acid distances. Grauer and Martin (2004),
kindly brought to our attention by Van Remsen, argued that such a date involved
erroneous precision, and that the date should be more accurately expressed as
338 to 288 mya. If we divide the 34.1% divergence between the two groups
mentioned above by 338, we get a rate of 0.10 pmy. If we divide it by 288 pmy,
we get a rate of 0.12 pmy. In these terms, the amino acid divergence between
Wandering AlbatrossDiomedea
exulansand Royal AlbatrossD. epomophoraof 1.32% indicates they diverged 12.1
mya +/- 1.1 my.

However, amino acid
distances that correspond to less than 1 to 2 million years are unreliable.
There are 300 bases involved with amino acids in the cytochrome-bgene, so that each change is about
0.0003. Obviously, on the time scales implied, the amino acid distances are a
blunt instrument compared with the cytochrome-bdistances. Presumably, there is a
margin of variance in changes to the amino acid bases. When we are talking
about divergences 12 mya, a difference of several hundred thousand years makes
little difference. But when we are talking about events less than a million
years ago, such a difference can be very significant. In contrast, the extreme
unlikelihood of any homoplasy in cytochrome-bon such a short time-scale makes it a
more reliable clock. Even if one wishes to dispute the bench-mark of 2% = 1mya,
the relative indications would still stand, which implies that the three taxa
in our data from thecautagroup diverged from each other
much more recently than any of the pairs involving what have traditionally been
considered distinct species.

Recommendation:

We believe that that our
evidence justifies the treatment ofcauta,eremita,salviniandsteadias a single species.

"The problems with use of mtDNA distances in defining species
limits are as follows:

"1. Coalescence. There can be mtDNA diversity within
populations. This throws a wrench in the works for dating recent divergences,
and it suggests that more than one individual per species must be sampled to
effectively apply genetic data to species limits questions.

"2. Phylogenetics. Modern phylogenetic methods do NOT use
distance matrices, contrary to the proposal. If one wants a distance matrix,
one can download the data from GenBank and generate one.

"3. mtDNA haplotype is one character among many, and provides
a very imprecise estimate of reproductive isolation. mtDNA is in no way known
to be involved in reproductive isolation. Clearly differentiated species of
rosy finches, red crossbills, and crowned sparrows share identical haplotypes
as a result of introgression or recent divergence (lack of lineage sorting). By
ignoring process and theory, the proposal's simple-minded speciation metric
cannot accommodate these cases.

"4. Cytochrome b actually suffers from homoplasy more than
most other mt genes, contrary to the proposal -- it's simply the most commonly
used because it was one of the first markers to be developed with universal
primers.

"5. Using an amino acid clock calibrated with a 200+myr old
calibration to date albatross subspecies divergences is fairly preposterous
(and this is coming from someone who's not afraid to go out on a limb with
calibration points)

"6. Molecular phylogenies frequently provide robust evidence
for generic realignments, even when they fail to provide a great deal of
evidence for species limits.

"7. Isolated cases of sympatry without interbreeding ARE
meaningful."

**********************************

Response from John
Penhallurick:

1. Of course it is desirable to have data
from several individuals within each population. We are working on obtaining
multiple samples from each taxon. But is it suggested that one should never
publish until one has absolutely complete data? Furthermore, we obtained most
of our data from sequences deposited with GenBank for Nunn and Stanley (1998).

2. What is done now is not the same as
what should or might be done.

3. The fact that mtDNA is not involved in
reproductive isolation is not the point. The point is that the extent of
sequence similarity between homologous genes in different species depends on
the length of time that has elapsed since the two species last had a common
ancestor. Taxa that have only recently diverged will have less difference than
taxa that diverged earlier. In our paper, we made the following statement:

In this communication, we follow the
Multidimensional BSC in maintaining the subspecies level to denominate young
evolutionary lines, when they are allopatric and do not differ substantially in
morphological or ecological terms.

Thus we were being consistent with this
view when we designatederemita,salviniandsteadias subspecies ofcauta.

It was suggested that differentiated
species of rosy finches, red crossbills, and crowned sparrows share identical
haplotypes as a result of introgression or recent divergence (lack of lineage
sorting). But a characteristic of Diomedeidae is remarkable fidelity to their
breeding islands. In this case, the probability of introgression being the
explanation of minimal or even zero differences in different albatross taxa
must be rated as virtually nil.

4. "Cytochrome-bactually suffers more from homoplasy
than most other mt genes" We grant that the rate of evolution of cyt-bis very rapid. Prychitko and Moore
(2000) stated: "Cytbevolves 2.8 times as fast as_-fibint7(14.0 times as fast at third codon
positions." It is that very fast rate of evolution that makes this gene useful
for examining closely related taxa, as opposed, say, to different families. But
homoplasy involves a minimum of two changes to a base at the same location. And
on average two changes at the same site must involve more time than a single
change at the same site. Over a long span of time (say 20 million years or
more) cyt-bdistances
become less reliable, certainly in terms of serving as a molecular clock. But
all the evidence indicates that in relation to thecautagroup (and equally to theDiomedea exulansandD.
epomophoragroups), we are
dealing with very recent divergences in evolutionary times. In the case ofD. epomophora epomophoraandD.
e. sanfordi the cyt-bdifference
is 0.0000%.D. exulans gibsonilikewise shows a difference of 0.0000%
fromD. e. antipodensis.
Does the anonymous commentator seriously suggest that such identity involves
homoplasy rather than recent divergence?

5. "Using an amino acid clock
calibrated with a 200+myr old calibration to date albatross subspecies is
fairly preposterous" This misrepresents totally what was actually said in
the proposal. I mentioned amino acid distances to make the point that our
calibration point in the 2004 paper was incorrect. But I specifically went on
to say that amino acid distances are useless for dating divergences in relation
to closely related albatross taxa. I reproduce what was said below:

Above, we have used cytochrome-bdistances to obtain estimates of time
of divergence between taxa. In our paper (2004), we used amino acid distances.
In the original paper, we used the widely accepted date of 310 mya for the
divergence date of diapsid reptiles and synapsid reptiles to calibrate our
amino acid distances. Grauer and Martin (2004), kindly brought to our attention
by Van Remsen, argued that such a date involved erroneous precision, and that
the date should be more accurately expressed as 338 to 288 mya. If we divide
the 34.1% divergence between the two groups mentioned above by 338, we get a
rate of 0.10 pmy. If we divide it by 288 pmy, we get a rate of 0.12 pmy. In
these terms, the amino acid divergence between Wandering AlbatrossDiomedea exulansand Royal AlbatrossD. epomophoraof 1.32% indicates they diverged 12.1
mya +/- 1.1 my.

However, amino acid distances that
correspond to less than 1 to 2 million years are unreliable. There are 300
bases involved with amino acids in the cytochrome-bgene, so that each change is about
0.0003. Obviously, on the time scales implied, the amino acid distances are a
blunt instrument compared with the cytochrome-bdistances. Presumably, there is a
margin of variance in changes to the amino acid bases. When we are talking
about divergences 12 mya, a difference of several hundred thousand years makes
little difference. But when we are talking about events less than a million
years ago, such a difference can be very significant. In contrast, the extreme
unlikelihood of any homoplasy in cytochrome-bon such a short time-scale makes it a
more reliable clock. Even if one wishes to dispute the bench-mark of 2% = 1mya,
the relative indications would still stand, which implies that the three taxa
in our data from thecautagroup diverged from each other
much more recently than any of the pairs involving what have traditionally been
considered distinct species.

6. "molecular phylogenies fail to
provide a great deal of evidence for species limits." Evidence that they
fail to provide evidence at the species level?

7. "Isolated cases of sympatry
without interbreeding are meaningful." What Alvaro stated was as follows:
"One pair ofsteadihas bred on the Forty-Fours (Chatham
Island group); this island is only a few km. from the Pyramid, which is the
breeding site of practically alleremita.
Asteadihas visited colonies ofsalvinion the Snares. A singlesalvinimade a nest in the main colony oferemita; I think it was by
itself, with no evidence of hybridization. One pair oferemitahas nested on the Snares, a breeding site
forsalvini. Some of these
sympatric breeding events have occurred for various years in a row."

To claim thatonepair ofsteadibreeding "only a few km from the
Pyramid" is strong evidence of reproductive isolation can only be called
staggering. Of thesteadi which
"has visited colonies on the Snares": we know nothing of the breeding
status of these birds. Were they immatures? When did they visit the colonies?Salvinistarts breeding in October, butsteadiin November. Likewise when did the
pair oferemitathat has nested on the Snares do so?Eremitabreeds Aug-Sept, whereassalvini breeds Oct-mid Nov.
Thus the significance of these isolated events is extremely problematic in
terms of any taxonomic significance.

In addition, we generated four Maximum
Parsimony (MP) trees that attempt to correct, to some extent, for differential
rates of evolution among different codon positions and
transitions/transversions. Since mtDNA changes at a faster rate than nuclear
DNA in genes (Meyer, 1994), this makes mitochondrial marker genes so useful for
the analysis of closely related taxa. But that same faster rate means that
beyond a time-scale of approximately 19 to 20 million years, multiple
substitutions in uncorrected data reduce the usefulness of mtDNA because of
homoplasy.

Accordingly, we generated four weighted MP
trees, with a view to clarifying deeper branching patterns within the
phylogenetic tree. We used the following weightings in connection with MP
analysis: a) omitting third codon positions altogether; b) down-weighting third
positions to 0.2, while weighting first and second positions at 1.0; c)
weighting transversions (that is, cases where a purine (adenine or guanine) is
substituted by a pyrimidine (cytosine or thymine) or vice versa) ten times more
than transitions (where a purine is replaced by the other purine, or a
pyrimidine by the other pyrimidine base); and d) weighting transversions three
times more than transitions. Of the four weighted trees, we place particular
emphasis on d), for the reason, as will become clear below, that in several
cases, it most accurately represents the differences between within-group and
between-group distance means in the matrix.

**********************************************************

Comments from Stiles: "NO. The previous
decision seems to have generated considerable heat, and as nobody else has come
forth with a contrary position, I shall take up Penhallurick's gauntlet. I
don«t claim to be an expert on molecular systematics, but I do have some
opinions regarding the role of molecular data - genetic distances in particular
- in deciding species limits. Basically, the essence of species is that they
act like species - that is, they don't interbreed when given the opportunity.
(The multidimensional species concept incorporates and extends
this argument). In this case, the opportunities evidently have existed, in
some cases repeatedly, with no interbreeding among these albatrosses. To me,
this is more telling evidence of species isolation than genetic distances.
Genetic distances calculated from particular genes (or from all the DNA, for
that matter) cannot ever be completely congruent with isolating mechanisms
unless one can show that the isolating mechanisms are the result of changes in
the particular gene (or chromosome) under study, which so far has only been
possible for things like polyploidy, chromosomal inversions etc., not single
genes like cytochrome b. Genes differ in mutation rates, but mutation rate
itself is a statistical property of genes and only becomes sufficiently
"clocklike" over sufficiently long time periods to permit stochastic
variability to average out. Unfortunately, the time frame for
speciation - the development of isolating mechanisms - often seems to fall in
the period of "lightning strikes" rather than the longer time frame
of "molecular clocks". Changes in external morphology, coloration
etc. also relate only approximately to isolating mechanisms as well as to
genetic distances - numerous cases of very different-looking birds
interbreeding happily exist. However, since mate choice often does involve
choices based upon external appearance, the relation between isolating
mechanisms and things like color or pattern is probably closer, on the whole,
than that between isolating mechanisms and genetic distances calculated from a
gene with no known connection to speciation, e. g., cytochrome b. The genetic
basis of isolating mechanisms is very poorly known in birds, but it seems
probable that such basis may differ markedly between particular cases - a
single, sexually-selected mutation could do it in one case, only gradual
accumulation of numerous mutations in another.. species are surely more
genetically different, on average, than subspecies or local populations, but
the zone of overlap is likely large enough that judging species limits solely
based on genetic distances is exceedingly risky, especially in slow-breeding
philopatric beasts of isolated colonies like albatrosses. This is not to
disqualify molecular data in determining relationships between taxa above the
species level - it is at these levels that such data are proving their great
value. The time frames involved tend to be longer and more
"clocklike", the process involved is simple divergence with time,
without the stochastic complications of isolating mechanisms at the core of
speciation."

Additional comments from
Frank Rheindt:

"In his new proposal to revert Alvaro's
Proposal #155 about albatross systematics, John Penhallurick extensively
resorts to his latest publication on genetic divergences of seabirds
(Penhallurick and Wink, 2004). Having written a reply to this publication
(Rheindt and Austin, 2005), and being the subject of a "Reply to the
Reply" that will be published shortly and that gives ample reference to
this present SACC Proposal, I would like to ask SACC to grant me the
opportunity of providing some input into its decision-making machinery in this
particular instance.

"Many of John Penhallurick's
arguments are contentious and open for discussion. For instance, he erroneously
ascribes biological significance to a pattern in which genetic divergences
between all former albatross subspecies fall below some gap, while those of
uncontested species fall above this gap. This and many other issues would be a
tempting subject of further discussion, but they distract from what is really
at the core of this problem. For what this proposal really boils down to is the
following question: Are those taxa of Shy Albatross really allopatric?

"I think we all agree in that there
is no regular hybridization or intergradation betweeneremita, salviniandcauta/steadi.
(Let's keep ill-definedsteaditogether withcautafor now). Even John Penhallurick
(involuntarily?) acknowledges this observation when he points to the strong
philopatry of albatrosses to defend the notion that small divergences could not
possibly be due to introgression. So if those taxa do not inter-breed, there is
only one question to answer: Are they allopatric? If they are not (as I am
arguing), all the divergences and distance measures put forth by John
Penhallurick automatically become immaterial to any discussion within the
confines of the BSC. As a self-confessed proponent of the multi-dimensional
BSC, John Penhallurick will agree that his divergence data can only serve as a
meaningful contribution in a situation where the taxa involved are allopatric.

"I contend that the three Shy
Albatross taxasalvini,
eremitaandcautaare not allopatric for the following
reasons:

"1.) Alvaro pointed to several
documented observations in which single individuals or pairs of one taxon ended
up in a colony of another taxon without inter-breeding. In some cases, the
"alien" pairs brought forth their own progeny, in others, the
individuals just hung around without mating. It is important to note that in
some cases this has happened for several years in a row, i.e. each year should
be counted as a separate instance in which the birds forewent an opportunity to
interbreed. John Penhallurick did not accord any significance to these
"isolated instances involving one or two birds", which surprises me,
considering that he later points out the strong philopatry of albatrosses as a
trait that will prevent them from ever displaying introgression. Albatrosses
are long-lived, slowly reproducing creatures with very low global populations.
With birds like that, "isolated instances" of hybridization (or the
lack thereof) are all we are ever going to see, and it would be quite out of
proportion to demand more. The evidence against hybridization isn't going to
get any better than that, and I find it remarkable that isolated pairs get lost
in the "wrong" colonies (and refuse to interbreed) at all,
considering that we are dealing with such strongly philopatric birds.

"2.) A couple of genetic studies into
albatross population structure have by now shown that some taxa are capable of
maintaining a panmictic population structure over the entire Southern Ocean
(Burg and Croxall 2001, 2004). The nominate Wandering Albatross (exulans)
for instance has a circumpolar range from the Falklands to near New Zealand and
has no discernible population subdivision, although some of its breeding
grounds are up to 7000km apart (with no land in between). At the Macquarie
Islands (NZ),exulansbreeds within 700km ofgibsoniandantipodensis,
a mere stone-throw in relative terms, and all three taxa can be seen foraging
in the same waters in between those islands. So keeping in mind thatexulansis capable of maintaining high gene
flow between Macquarie and Kerguelen (7000km), I am certain they would have
started hybridizing withgibsoni/antipodensis
a long time ago if they had decided they belong to the same biological
species.

"3.) In Shy Albatrosses, the picture
is a little more complicated, to be fair, because all taxa are of relatively
restricted breeding distribution around New Zealand. However, Alvaro already
mentioned their great dispersal potential when he pointed out thatsalvini(normally breeding on the Snares and
Bounties, NZ) established a colony on the Crozets, which is - to be precise -
more than 16 times the distance between the Snares and Bounties when measured
across Antarctica, or more than 20 times that distance when measured along the
same latitude (a more likely dispersal scenario). On their way to the new
colony,salviniindividuals would have hopped across
the home range of at leastcauta,
if notcauta, eremita andsteadi. But "hopping
across the ranges of neighbors" is a misleading concept when talking about
albatrosses, and that is exactly the point: The New Zealand home sector of all
Shy Albatross taxa is so tiny in comparison with their true dispersal potential
as to render all these taxa essentially non-allopatric. Consider Figure 1 (see
below), in which all the breeding locations around New Zealand are depicted.
The taxa do not fall into geographic clusters, but their breeding islands are distributed
in a seemingly random manner around New Zealand, with some breeding islands
being much closer to the colonies of other taxa. Now additionally consider that
two of these taxa, namelysalviniandcauta/steadi(I prefer to lumpcautaandsteadiinto one entity for convenience for
now) also maintain breeding colonies far outside this map. Given this seemingly
random and interspersed breeding distribution, the great dispersal potential of
these birds and their regular contact, I have not the slightest doubt that they
would have started to interbreed a long time ago, if it weren't for some
isolation mechanism that prevents them from doing so.

"4.) Last but not least, let's take
into consideration what genetic work has been done on Shy Albatrosses themselves.
Unfortunately, Abbott and Double (2003a, b) have looked at microsatellites and
mitochondrial control region of onlysteadiandcauta,
the two least differentiated taxa, which almost everyone (incl Alvaro, John
Penhallurick and myself) would opt to retain in one species. In fact,steadiis poorly defined morphologically and
its invalidity has been brought up repeatedly. Even so, Abbott and Double have
shown thatsteadi andcautaare demographically isolated from each
other and they have not detected any signs of recent gene flow. If there is no
recent gene flow betweencautaand ill-definedsteadi, wouldn't it be sound to
assume that there is even less a case for gene flow between the morphologically
well-separatederemita,salviniandcauta/steadi?
I acknowledge that Abbott and Double's studies are not as crucial to our
taxonomic question as many people would like to make them appear, but we have
got to go with what is published, and I do think these studies put the burden
of proof on anyone who would contend that there is gene flow between our three
taxa.

"In view of the non-allopatry of
these three taxa, and in view of the lack of hybridization despite ample
potential to hybridize, I would thus suggest that we are dealing with three
biological species. I think the only way to convince me otherwise would be the
demonstration of gene flow and hybridization between those taxa. This could
either be done through a detailed study into the population genetics of these
taxa, or through the documentation of occurrences of hybridization. The
standards for splitting remain high: A handful of cases of successful
hybridization would be enough to make most people happy to re-consider the
case, I guess"

Comments from Jaramillo: "NO - There is a
lot of interesting information and discussion here, and I think it's wonderful
that we have gotten this level of involvement from some of the people directly
working on this issue. I don't think I can add anything that has not been said
before on this topic, and I think that Frank Rheindt makes some very important
points and frames this problem in a clearer way than I had thought about it
before. Yes, really these taxa of albatrosses are functionally sympatric, and
there is no evidence they interbreed. These taxa are reproductively isolated,
although they reasonable opportunities to interbreed, they do not."

Additional comments from
Penhallurick: "Rheindt
and Austin cite specifically Abbott and Double (2003 a, b); and Burg and
Croxall (2001,2004) as studies that have "uncovered new evidence for the
species status of at least some of these forms". In what we say about
these sources, we wish to stress that we are not denying the value of the work
of Abbott and Double in revealing important information about gene flows between
the populations ofcautaalbatrosses, and on speciation
processes. But we do not believe that anything in Abbott and Double's two
papers is relevant to the question we address here: should a number of taxa
traditionally treated as subspecies within a single species be treated as
comprising two or more species. Of critical importance in this discussion are
the species concepts utilised in these studies.

"Abbott and Double (2003a) state at
the beginning: "In accordance with the most recent taxonomic hypothesis
available for albatrosses, and for ease of discussion in this paper, we have
adopted the species nomenclature suggested by Robertson & Nunn (1998). We
use the names "shy albatross" and "white-capped albatross"
and refer to them as species, although our aim is to investigate the
appropriateness of this classification." Since Robertson and Nunn (1998)
explicitly said that they were working within the Phylogenetic Species Concept,
and since Robertson and Nunn's paper was not published in a refereed journal, this
is not a promising beginning for any discussion in accordance with the
Multidimensional BSC or the Evolutionary Species Concept (ESC). Another point
about Abbott and Double (2003a) is that their results were based on a 299 base
pair fragment of Domain I of the mitochondrial control region. Thus their
results are not directly comparable with our results, which are based on 1143
base pairs from mtDNA cytochrome-b. In their abstract, Abbott and Double
(2003a) stated concisely: 'Low sequence divergence between shy and white-capped
albatrosses (1.8%) and between their close relatives, Salvin's and Chatham
albatrosses (2.9%), was observed. Much higher sequence divergence was found
between the shy/white-capped pair and the Salvin's/Chatham pair (7.0%). Phylogenetic
analyses confirmed the separation of the shy/white-capped pair and the
Salvin's/Chatham pairbut did
not provide species-level resolution.' (Emphasis added).

"The abstract for Abbott and Double
(2003b) refers to "áthe closely related shy albatross (Thalassarche
cauta) and white-capped albatross (Thalassarche steadi)" and
reported "álevels of genetic differentiation between the species, and
among three populations within each species". However, there is in fact no
evidence brought forward in the paper as to whether these taxa should be
treated at the species or subspecies level. They stated elsewhere in the
abstract: "These results formed the basis for the recommendation that the
three white-capped albatross populations (as a whole) and each shy albatross
population be treated as separate units for conservation." We do not
disagree in any way that each of the taxa should be a focus of conservation
efforts; but as we stated in our (2004) paper, conservation concerns should not
dictate species concepts. In conclusion, we could find no evidence of any data
or argument relevant to the species/subspecies question in either paper by
Abbott and Double.

"Burg and Croxall (2001) was
discussed in Penhallurick and Wink (2004). This paper dealt with the relationships
and classification ofThalassarche
chrysostoma(J. R. Forster
1785) Grey-headed Albatross andThalassarche
melanophris(Temminck 1828)
Black-browed Albatross. In terms of what species concept they were using, they
cite Moritz (1994a and 1994b), who described the differences between management
units (MU) and evolutionary significant units (ESU): ESUs are two groups that
show reciprocal monophyly of mtDNA haplotypes and significant differences in
allele frequencies at nuclear loci. MUs on the other hand show significant
differences in allele frequencies without regard to the phylogeny of the
markers. They also cite Avise & Wollenberg (1997), who endorsed the
Phylogenetic Species Concept (PSC) which emphasizes the criteria of
phylogenetic relationships and not reproductive relationships.

"Their final conclusion in relation
toThalassarche melanophriswas as follows:

'For black-browed albatrosses, the genetic distinctiveness ofT. impavidaconfirms recent views that despite
hybridization, this taxon merits species recognition. The degree of genetic
differentiation between the Falkland Island population and the otherT. melanophriswas unexpected. If morphological,
morphometric and/or ecological distinctions from the largerT. melanophrispopulation can be discerned, then this
taxon might also be awarded species status. As it stands, it is a very strong
candidate for distinct subspecific status and qualified using either the ESU or
PSU criteria.' Thus it appears that they are using either the ESU model, which stresses
conservation values, or the PSC, which as we know treats all subspecies as good
species. Since we reject both species concepts, this can not be considered
strong evidence against our analysis.

"The main conclusion of Burg and
Croxall (2004) is stated thus:
Both our mtDNA, microsatellite results indicate that wandering albatrosses from
the Atlantic/Indian Group (D. exulans) form one Evolutionarily
Significant Unit (ESU; Moritz 1994a) and the birds from the New Zealand group (D.
antipodensis/D. gibsoni) form a second ESU. Although we only have
mtDNA data from a small number of samples from the Tristan group (D.
dabbenena; n = 3), the level of mtDNA divergence between it and other
members of the complex suggests that these birds should be treated as a third
ESU. Because wandering albatrosses from Antipodes (D. antipodensis) and
Adams Islands (D. gibsoni) show significant differences from each other
in terms of microsatellite allele frequencies and mtDNA data, but no fixed
mtDNA differences, birds from these two islands should form two Management
Units (MU, Moritz 1994). This is also logical in the light of their very
different ranges at sea, especially wintering areas, which are likely to
necessitate different management strategies.

"It is clear that the species concept
that is operating here is that of the conservation-oriented ESU of Moritz
(1994a), and that in our terms, it is not relevant to the species/subspecies
issue for these taxa.

"An important contribution to the
debate about species/subspecies is the paper by Helbig et al. (2002). In terms
of species concepts, they generally endorse the Evolutionary Species Concept
(Mayden 1997) and the very similar General Lineage Concept (de Queiroz 1998,
1999), which state that species are evolutionary lineages that maintain their
integrity (with respect to other such lineages) through time and space. They
also stated that the Biological Species Concept (and we assume that they are
referring to the Multidimensional version of the BSC, since the Non-Dimensional
version of the BSC applies only to sympatric populations) "from its
theoretical backgroundáis entirely compatible with the ESC." Helbig et al.
(2002) further stated: "It is this point - implicit predictions about the
future š where species concepts differ, and we have to make a decision: do we
want to call any recognizable population a species no matter how likely it is
that it may fuse with other populations once they come into contact? Or do we
want to call "species" only those taxa for which we feel reasonably
certain that they will retain their integrity, no matter what other taxa they
may encounter in the future? For the purposes of recommending a practical
taxonomy of West Palearctic birds, we have opted for the latter. We believe
that taxa should only be assigned species rank if they have diverged to the
extent that merging of their gene pools in the future is unlikely."

"They also distinguish between the
conditions relating to sympatry, parapatry and allopatry, and conclude:
'allopatric taxa will be assigned species rank if:

4.1 they are fully diagnosable in each ofseveraldiscrete or continuously varying
characters related to different functional contexts, e. g. structural features
(often related to foraging strategy), plumage colours, vocalisations (both
often related to mate recognition) or DNA sequences, and the sum of the
character differences corresponds to or exceeds the level of divergence seen in
related species that coexist in sympatry.'

"The matrix of Tamura-Nei distances
for all albatrosses can be found at

"The gap between 1.72% and 1.08% is
the largest in the dataset. It seems sensible to treat this gap as that
cut-off, below which, we are dealing with subspecies, and above which, we are
dealing with separate species. We stress that there is no strong evidence that
contradicts this proposal. We concede thatsalvinianderemitahave diverged furthest from nominate cautaamong all the subspecies within the
genusThalassarche. But
classification implies the imposition of boundaries on what in reality is a
continuum. With our data, it makes no sense to claim thatsalvinianderemitashould be separated at the specific
level.

"Our data suggest even less the
validity of splitting eitherDiomedea
exulansorDiomedea epomophora. We note that
the clades containing taxa within theD.
exulanscomplex in the phylogram
in Figure 2 are very shallow. The Tamura-Nei distance between nominateepomophoraandsanfordiis 0.0000%, and the same distance is found
betweenD. e. gibsoni andD. e. antipodensis. This figure
suggests that the divergence between these taxa was very recent. Whereas Burg
and Croxall (2004), in terms of "ESUs", suggested splitting exulansfromantipodensis/gibsoniand both fromdabennena, the TN distances of
0.902% between nominateexulansanddabbenena;
of 0.539% betweenexulansandantipodensis;
of 0.539% betweenexulansandgibsoni;
of 0.540% betweenexulansandamsterdamensis;
is well below the 1.72% which was the lowest figure between traditional species
in Thalassarche. As compared with the TN distance betweenexulansandepomophoraof 3.797%, these data suggest that in
terms of either the Multidimensional BSC or ESC, we have only two species:D. exulansandD.
epomophora."